Sensory stimulus-evoked neural oscillations have been described in many animals. For a particular modality in a given species, oscillation frequency often seems unrelated to stimulus intensity. In the locust olfactory system, for example, odors elicit 20 Hz oscillations that vary little in frequency even when odor concentration varies over 5 orders of magnitude. In some cases, though, stimulus intensity does appear to modulate oscillation frequency;the changing velocity of a visual stimulus, for example, can systematically change the frequency of gamma oscillations in the cat visual cortex. What determines the properties of these oscillations? What can an analysis of these properties tell us about ways stimulus intensity is encoded by neurons? Here, we used the insect olfactory system to clarify the encoding of odor intensity, and the relationship between stimulus intensity and oscillation frequency. In insects, odor molecules are first detected by olfactory receptor neurons. Axons from these receptors converge upon glomeruli in the antennal lobe (analogous to the vertebrates olfactory bulb) where excitatory projection neurons (analogous to mitral cells) and mainly inhibitory local interneurons interact. Projection neurons send excitatory inputs to local neurons, and local neurons send rapid inhibitory feedback to projection neurons via GABAA-like receptors. In insects, this feedback circuit has been shown to synchronize groups of projection neurons, resulting in regular oscillating waves of output that depolarize follower neurons downstream that in many ways resemble those of the vertebrate pyriform cortex. The oscillatory waves can be detected as a local field potential. We found that odors evoked oscillatory responses in the moth Manduca sexta. Further, in the moth, we found that lengthy odor pulses evoked oscillations that began at 40 Hz but then suddenly decreased to 15-20 Hz. Simultaneous local field potential recordings and recordings from the moths antenna showed the net response intensity of receptor neurons decreased in parallel to the shift in oscillation frequency. This suggested oscillation frequency might be determined by the intensity of the response of the receptor neuron population. In apparent contradiction, though, we also found that odor-evoked oscillation frequency remained remarkably constant across a broad range of odor concentrations. What then is the relationship between stimulus intensity and oscillation frequency? Our approach, combining experimental and computational methods, led to several conclusions. First, we found the frequency of odor-evoked oscillations in the moth olfactory system is determined by the intensity of input to the oscillatory AL network, but this intensity is determined by sensory adaptation and saturation of receptor neurons rather than by the intensity of olfactory stimuli. Second, extending prior work, we demonstrated that the vast majority of olfactory dynamic range is encoded in the periphery by the number of responsive receptor neurons rather than by the firing rates of those receptor neurons. And third, we characterized a new stable oscillatory regime in which principle neurons participating in an oscillatory network can fire much faster than the oscillation frequency.
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